Skip to main content
NCBI home page
The Journal of General Physiology logoLink to The Journal of General Physiology
. 1978 Apr 1;71(4):369–396. doi: 10.1085/jgp.71.4.369

Visual pigment and photoreceptor sensitivity in the isolated skate retina

PMCID: PMC2215732  PMID: 660156

Abstract

Photoreceptor potentials were recorded extracellularly from the aspartate-treated, isolated retina of the skate (Raja oscellata and R. erinacea), and the effects of externally applied retinal were studied both electrophysiologically and spectrophotometrically. In the absence of applied retinal, strong light adaptation leads to an irreversible depletion of rhodopsin and a sustained elevation of receptor threshold. For example, after the bleaching of 60% of the rhodopsin initially present in dark-adapted receptors, the threshold of the receptor response stabilizes at a level about 3 log units above the dark-adapted value. The application of 11-cis retinal to strongly light-adapted photoreceptors induces both a rapid, substantial lowering of receptor threshold and a shift of the entire intensity-response curve toward greater sensitivity. Exogenous 11-cis retinal also promotes the formation of rhodopsin in bleached photoreceptors with a time-course similar to that of the sensitization measured electrophysiologically. All-trans and 13-cis retinal, when applied to strongly light-adapted receptors, fail to promote either an increase in receptor sensitivity or the formation of significant amounts of light-sensitive pigment within the receptors. However, 9-cis retinal isin. These findings provide strong evidence that the regeneration of visual pigment in the photoreceptors directly regulates the process of photochemical dark adaptation.

Full Text

The Full Text of this article is available as a PDF (1.4 MB).

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Arden G. B. Voltage gradients across the receptor layer of the isolated rat retina. J Physiol. 1976 Apr;256(2):333–360.1. doi: 10.1113/jphysiol.1976.sp011328. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. BROWN P. K., WALD G. The neo-b isomer of vitamin A and retinene. J Biol Chem. 1956 Oct;222(2):865–877. [PubMed] [Google Scholar]
  3. Beatty D. D. Visual pigments of 3 species of cartilaginous fishes. Nature. 1969 Apr 19;222(5190):285–285. doi: 10.1038/222285a0. [DOI] [PubMed] [Google Scholar]
  4. Bownds D., Brodie A. E. Light-sensitive swelling of isolated frog rod outer segments as an in vitro assay for visual transduction and dark adaptation. J Gen Physiol. 1975 Oct;66(4):407–425. doi: 10.1085/jgp.66.4.407. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Bridges C. D. Rhodopsin regeneration in rod outer segments: utilization of 11-cis retinal and retinol. Exp Eye Res. 1977 Jun;24(6):571–580. doi: 10.1016/0014-4835(77)90114-2. [DOI] [PubMed] [Google Scholar]
  6. Bridges C. D. Vitamin A and the role of the pigment epithelium during bleaching and regeneration of rhodopsin in the frog eye. Exp Eye Res. 1976 May;22(5):435–455. doi: 10.1016/0014-4835(76)90182-2. [DOI] [PubMed] [Google Scholar]
  7. Brin K. P., Ripps H. Rhodopsin photoproducts and rod sensitivity in the skate retina. J Gen Physiol. 1977 Jan;69(1):97–120. doi: 10.1085/jgp.69.1.97. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Brodie A. E., Bownds D. Biochemical correlates of adaptation processes in isolated frog photoreceptor membranes. J Gen Physiol. 1976 Jul;68(1):1–11. doi: 10.1085/jgp.68.1.1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Brown P. K. Rhodopsin rotates in the visual receptor membrane. Nat New Biol. 1972 Mar 15;236(63):35–38. doi: 10.1038/newbio236035a0. [DOI] [PubMed] [Google Scholar]
  10. Clusin W. T., Bennett M. V. Calcium-activated conductance in skate electroreceptors: current clamp experiments. J Gen Physiol. 1977 Feb;69(2):121–143. doi: 10.1085/jgp.69.2.121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Cone R. A., Brown P. K. Spontaneous regeneration of rhodopsin in the isolated rat retina. Nature. 1969 Mar 1;221(5183):818–820. doi: 10.1038/221818a0. [DOI] [PubMed] [Google Scholar]
  12. Cone R. A., Cobbs W. H., 3rd Rhodopsin cycle in the living eye of the rat. Nature. 1969 Mar 1;221(5183):820–822. doi: 10.1038/221820a0. [DOI] [PubMed] [Google Scholar]
  13. DOWLING J. E. Chemistry of visual adaptation in the rat. Nature. 1960 Oct 8;188:114–118. doi: 10.1038/188114a0. [DOI] [PubMed] [Google Scholar]
  14. DOWLING J. E. NEURAL AND PHOTOCHEMICAL MECHANISMS OF VISUAL ADAPTATION IN THE RAT. J Gen Physiol. 1963 Jul;46:1287–1301. doi: 10.1085/jgp.46.6.1287. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Dowling J. E., Ripps H. Adaptation in skate photoreceptors. J Gen Physiol. 1972 Dec;60(6):698–719. doi: 10.1085/jgp.60.6.698. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Dowling J. E., Ripps H. S-potentials in the skate retina. Intracellular recordings during light and dark adaptation. J Gen Physiol. 1971 Aug;58(2):163–189. doi: 10.1085/jgp.58.2.163. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Dowling J. E., Ripps H. The proximal negative response and visual adaptation in the skate retina. J Gen Physiol. 1977 Jan;69(1):57–74. doi: 10.1085/jgp.69.1.57. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Dowling J. E., Ripps H. Visual adaptation in the retina of the skate. J Gen Physiol. 1970 Oct;56(4):491–520. doi: 10.1085/jgp.56.4.491. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Ernst W., Kemp C. M. Scotopic and photopic dark adaptation of the b wave isolated rat retina. Nature. 1975 Nov 13;258(5531):170–171. doi: 10.1038/258170a0. [DOI] [PubMed] [Google Scholar]
  20. Ernst W., Kemp C. M. The effects of rhodopsin decomposition on P3 responses of isolated rat retinae. Vision Res. 1972 Dec;12(12):1937–1946. doi: 10.1016/0042-6989(72)90050-8. [DOI] [PubMed] [Google Scholar]
  21. Fain G. L., Dowling J. E. Intracellular recordings from single rods and cones in the mudpuppy retina. Science. 1973 Jun 15;180(4091):1178–1181. doi: 10.1126/science.180.4091.1178. [DOI] [PubMed] [Google Scholar]
  22. Frank R. N. Properties of "neural" adaptation in components of the frog electroretinogram. Vision Res. 1971 Oct;11(10):1113–1123. doi: 10.1016/0042-6989(71)90115-5. [DOI] [PubMed] [Google Scholar]
  23. Grabowski S. R., Pak W. L. Intracellular recordings of rod responses during dark-adaptation. J Physiol. 1975 May;247(2):363–391. doi: 10.1113/jphysiol.1975.sp010936. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Grabowski S. R., Pinto L. H., Pak W. L. Adaptation in retinal rods of axolotl: intracellular recordings. Science. 1972 Jun 16;176(4040):1240–1243. doi: 10.1126/science.176.4040.1240. [DOI] [PubMed] [Google Scholar]
  25. Green D. G., Dowling J. E., Siegel I. M., Ripps H. Retinal mechanisms of visual adaptation in the skate. J Gen Physiol. 1975 Apr;65(4):483–502. doi: 10.1085/jgp.65.4.483. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Hecht S. THE DARK ADAPTATION OF THE HUMAN EYE. J Gen Physiol. 1920 May 20;2(5):499–517. doi: 10.1085/jgp.2.5.499. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Hood D. C., Hock P. A., Grover B. G. Dark adaptation of the frog's rods. Vision Res. 1973 Oct;13(10):1953–1963. doi: 10.1016/0042-6989(73)90066-7. [DOI] [PubMed] [Google Scholar]
  28. Hubbard R., Bownds D., Yoshizawa T. The chemistry of visual photoreception. Cold Spring Harb Symp Quant Biol. 1965;30:301–315. doi: 10.1101/sqb.1965.030.01.032. [DOI] [PubMed] [Google Scholar]
  29. Hubbard R., Kropf A. THE ACTION OF LIGHT ON RHODOPSIN. Proc Natl Acad Sci U S A. 1958 Feb;44(2):130–139. doi: 10.1073/pnas.44.2.130. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Huddleston S. K., Williams T. P. Physiological activity of isorhodopsin in rat rods. Vision Res. 1977;17(6):711–714. doi: 10.1016/s0042-6989(77)80007-2. [DOI] [PubMed] [Google Scholar]
  31. Keirns J. J., Miki N., Bitensky M. W., Keirns M. A link between rhodopsin and disc membrane cyclic nucleotide phosphodiesterase. Action spectrum and sensitivity to illumination. Biochemistry. 1975 Jun 17;14(12):2760–2766. doi: 10.1021/bi00683a032. [DOI] [PubMed] [Google Scholar]
  32. Kleinschmidt J., Dowling J. E. Intracellular recordings from gecko photoreceptors during light and dark adaptation. J Gen Physiol. 1975 Nov;66(5):617–648. doi: 10.1085/jgp.66.5.617. [DOI] [PMC free article] [PubMed] [Google Scholar]
  33. MATTHEWS R. G., HUBBARD R., BROWN P. K., WALD G. TAUTOMERIC FORMS OF METARHODOPSIN. J Gen Physiol. 1963 Nov;47:215–240. doi: 10.1085/jgp.47.2.215. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Matsuura T. Rod late receptor potential and rhodopsin concentration of an isolated frog retina. Jpn J Physiol. 1975;25(2):123–133. doi: 10.2170/jjphysiol.25.123. [DOI] [PubMed] [Google Scholar]
  35. NOELL W. K. The origin of the electroretinogram. Am J Ophthalmol. 1954 Jul;38(12):78–90. doi: 10.1016/0002-9394(54)90012-4. [DOI] [PubMed] [Google Scholar]
  36. Naka K. I., Rushton W. A. S-potentials from luminosity units in the retina of fish (Cyprinidae). J Physiol. 1966 Aug;185(3):587–599. doi: 10.1113/jphysiol.1966.sp008003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Normann R. A., Werblin F. S. Control of retinal sensitivity. I. Light and dark adaptation of vertebrate rods and cones. J Gen Physiol. 1974 Jan;63(1):37–61. doi: 10.1085/jgp.63.1.37. [DOI] [PMC free article] [PubMed] [Google Scholar]
  38. Ostroy S. E. Hydrogen ion changes of rhodopsin. pK changes and the thermal decay of metarhodopsin II380. Arch Biochem Biophys. 1974 Sep;164(1):275–284. doi: 10.1016/0003-9861(74)90032-0. [DOI] [PubMed] [Google Scholar]
  39. Pepperberg D. R., Lurie M., Brown P. K., Dowling J. E. Visual adaptation: effects of externally applied retinal on the light-adapted, isolated skate retina. Science. 1976 Jan 30;191(4225):394–396. doi: 10.1126/science.1246621. [DOI] [PubMed] [Google Scholar]
  40. RUSHTON W. A. Rhodopsin measurement and dark-adaptation in a subject deficient in cone vision. J Physiol. 1961 Apr;156:193–205. doi: 10.1113/jphysiol.1961.sp006668. [DOI] [PMC free article] [PubMed] [Google Scholar]
  41. RUSHTON W. A. STRAY LIGHT AND THE MEASUREMENT OF MIXED PIGMENTS IN THE RETINA. J Physiol. 1965 Jan;176:46–55. doi: 10.1113/jphysiol.1965.sp007534. [DOI] [PMC free article] [PubMed] [Google Scholar]
  42. Shichi H., Somers R. L. Possible involvement of retinylidene phospholipid in photoisomerization of all-trans-retinal to 11-cis-retinal. J Biol Chem. 1974 Oct 25;249(20):6570–6577. [PubMed] [Google Scholar]
  43. Sillman A. J., Ito H., Tomita T. Studies on the mass receptor potential of the isolated frog retina. I. General properties of the response. Vision Res. 1969 Dec;9(12):1435–1442. doi: 10.1016/0042-6989(69)90059-5. [DOI] [PubMed] [Google Scholar]
  44. Steinberg R. H., Schmidt R., Brown K. T. Intracellular responses to light from cat pigment epithelium: origin of the electroretinogram c-wave. Nature. 1970 Aug 15;227(5259):728–730. doi: 10.1038/227728a0. [DOI] [PubMed] [Google Scholar]
  45. Tokunaga F., Kawamura S., Yoshizawa T. Analysis by spectral difference of the orientational change of the rhodopsin chromophore during bleaching. Vision Res. 1976;16(6):633–641. doi: 10.1016/0042-6989(76)90011-0. [DOI] [PubMed] [Google Scholar]
  46. WALD G., BROWN P. K., GIBBONS I. R. The problem of visual excitation. J Opt Soc Am. 1963 Jan;53:20–35. doi: 10.1364/josa.53.000020. [DOI] [PubMed] [Google Scholar]
  47. WALD G., BROWN P. K. Human rhodopsin. Science. 1958 Jan 31;127(3292):222–226. doi: 10.1126/science.127.3292.222. [DOI] [PubMed] [Google Scholar]
  48. WALD G., BROWN P. K., SMITH P. H. Iodopsin. J Gen Physiol. 1955 May 20;38(5):623–681. doi: 10.1085/jgp.38.5.623. [DOI] [PMC free article] [PubMed] [Google Scholar]
  49. WALD G., BROWN P. K. The role of sulfhydryl groups in the bleaching and synthesis of rhodopsin. J Gen Physiol. 1952 May;35(5):797–821. doi: 10.1085/jgp.35.5.797. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. WEALE R. A. RELATION BETWEEN DARK ADAPTATION AND VISUAL PIGMENT REGENERATION. J Opt Soc Am. 1964 Jan;54:128–129. doi: 10.1364/josa.54.000128. [DOI] [PubMed] [Google Scholar]
  51. Wald G., Brown P. K. The Synthesis of Rhodopsin from Retinene(1). Proc Natl Acad Sci U S A. 1950 Feb;36(2):84–92. doi: 10.1073/pnas.36.2.84. [DOI] [PMC free article] [PubMed] [Google Scholar]
  52. Wald G. Molecular basis of visual excitation. Science. 1968 Oct 11;162(3850):230–239. doi: 10.1126/science.162.3850.230. [DOI] [PubMed] [Google Scholar]
  53. Weinstein G. W., Hobson R. R. Adaptation in the isolated rat retina. Nature. 1970 Aug 29;227(5261):957–959. doi: 10.1038/227957a0. [DOI] [PubMed] [Google Scholar]
  54. Weinstein G. W., Hobson R. R., Dowling J. E. Light and dark adaptation in the isolated rat retina. Nature. 1967 Jul 8;215(5097):134–138. doi: 10.1038/215134a0. [DOI] [PubMed] [Google Scholar]
  55. Wiggert B. O., Chader G. J. A receptor for retinol in the developing retina and pigment epithelium. Exp Eye Res. 1975 Aug;21(2):143–151. doi: 10.1016/0014-4835(75)90078-0. [DOI] [PubMed] [Google Scholar]
  56. Witkovsky P., Dudek F. E., Ripps H. Slow PIII component of the carp electroretinogram. J Gen Physiol. 1975 Feb;65(2):119–134. doi: 10.1085/jgp.65.2.119. [DOI] [PMC free article] [PubMed] [Google Scholar]
  57. Witkovsky P., Gallin E., Hollyfield J. G., Ripps H., Bridges C. D. Photoreceptor thresholds and visual pigment levels in normal and vitamin A-deprived Xenopus tadpoles. J Neurophysiol. 1976 Nov;39(6):1272–1287. doi: 10.1152/jn.1976.39.6.1272. [DOI] [PubMed] [Google Scholar]
  58. Witkovsky P., Nelson J., Ripps H. Action spectra and adaptation properties of carp photoreceptors. J Gen Physiol. 1973 Apr;61(4):401–423. doi: 10.1085/jgp.61.4.401. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Zimmerman W. F. The distribution and proportions of vitamin A compounds during the visual cycle in the rat. Vision Res. 1974 Sep;14(9):795–802. doi: 10.1016/0042-6989(74)90143-6. [DOI] [PubMed] [Google Scholar]

Articles from The Journal of General Physiology are provided here courtesy of The Rockefeller University Press

RESOURCES